A Pesticide Decision-Making Guide to Protect Pollinators in
Tree Fruit Orchards
By Maria van Dyke, Emma Mullen, Dan Wixted, and Scott McArt
2018 Edition
Pollinator Network at Cornell, 2018 Cornell University, Department Of Entomology
Contents
Choosing lower-risk pesticides for pollinators in New York orchards 1
How to use this guide 3
Understanding the terms in this guide 4
EPA Pesticide toxicity standards 4
Synergistic Interactions 4
Systemic Pesticides 4
Adjuvants and/or inert ingredients 5
Tying it all together: adopting an Integrated Pest and Pollinator Management (IPPM) approach 5
IPPM: Putting the “pollinator” in IPM: 6
Table 1: Product formulations and their active ingredients 7
Table 2: Pesticide synergies and acute, chronic, and sublethal toxicities for honey bees and other
pollinators 9
Literature cited 24
Appendix A: Pollination contract ______________________________________________________ 28
Acknowledgments This research and development of this guide was supported by the New York State Environmental
Protection Fund and New York Farm Viability Institute grant FOC 17-001. The expert advice and consultation provided by Dan Wixted of the Cornell Pesticide Management Education Program was
supported by the Crop Protection and Pest Management Extension Implementation Program [grant no. 2017-70006-27142/project accession no. 1014000] from the USDA National Institute of Food and Agriculture.
Download this guide for free from: https://pollinator.cals.cornell.edu/resources/grower-resources/
Choosing lower-risk pesticides for pollinators in New York orchards Growers recognize the vital role of pollination and understand that managing pests while protecting
pollinators can be a balancing act. Both components are essential for a successful harvest, yet they can
sometimes be in conflict with one another. Pollinators (mostly bees) are busy pollinating orchard
blossoms at the same time growers need to be managing specific pests and diseases. The impact of
pesticides on pollinator health has been an active area of research in recent years, including work
conducted in New York orchards and elsewhere. The results from this research are clear: Pesticides can
be a threat to pollinators, but there is variation in risk, due in part to grower management practices.
This guide summarizes known impacts of pesticides on bees in a clear, concise, easy-to-use format. Our
goal is to provide information to growers so they can develop an effective Integrated Pest and Pollinator
Management program.
Pesticide risk to pollinators comes from a
combination of exposure and effects.
Pollinators may be exposed to pesticides
through direct sprays, puddle water,
guttation droplets, extrafloral nectaries,
pollen and nectar from treated crops and
surrounding wildflowers, and residues
that accumulate in soil (for ground nesting
bees). Pesticides have an effect on
pollinators if exposure is sufficient to
cause lethal or sub-lethal impacts.
Recently, an understanding of the
interactions between pesticides on bee
health has brought focus on active
ingredients that synergize, meaning that
the combined toxicity is greater than the
sum of the toxicity of each pesticide applied separately. Pesticide risk studies find that synergies among
different pesticides can increase the toxicity of some pesticides up to 1000-fold. While some synergies
are intentional and make a higher efficacy formulation for the pests they are meant to control, many
synergies can lead to unintentional combined effects that can substantially increase pesticide risk to
bees. These synergies are beyond the scope of EPA label guidelines.
In summary, 47 of the 140 chemicals listed in this guide have been shown to synergize with other
agrochemicals in tank mixes, formulations, or on plant or soil surfaces. These chemicals include some
fungicides, neonicotinoids, pyrethroids, carbamates, organophosphates , piperonyl butoxide and some
adjuvants. Synergisms are noted with a in Table 2, ‘Synergies and acute, chronic, and sublethal
toxicities for honey bees and other pollinators.’
©C
Kit
chen
A native Andrena species grooming cherry pollen from its face.
1
This guide summarizes reported pesticide effects as of October 2018. The guide presents the most up-to-date information about the impacts of fungicides, insecticides, microbicides, and growth regulators on bees that pollinate tree fruits. New York is home to 416 species of bees, and over 120 species are known
to be important for NYS apple pollination, with several of those species also visiting other tree fruits.
It is well documented that each bee species can respond differently to active ingredients. However,
there are so many bee species, each differing with respect to physiology, sociality, nesting habits,
foraging habits, and ability to tolerate pesticides, that it is unrealistic to determine how every use of
every pesticide will affect each species. Therefore,
the Environmental Protection Agency (EPA) uses acute toxicity to honey bees (Apis mellifera) as a
proxy for the potential adverse effects of a pesticide on bees in general, but will at times take studies on
other bee species into account as appropriate. In addition to presenting these EPA toxicity ratings, this
guide specifically highlights the chemical combinations that produce synergistic effects on bee
pollinators. Furthermore, we expand on EPA standards to include reports of sublethal effects in
honey bees as well as acute, chronic, and sublethal effects on bumble bee and solitary bee species. Chronic and sublethal effects include reduced reproduction, size, immunity, and negative effects on bee behaviors such as cleaning, nesting, foraging, and flying.
This guide is intended to be used as a decision-
making tool. The primary goal of this guide is to help
growers understand and compare the acute toxicity and synergistic effects of different pesticides on
pollinators. The majority of registered products for New York orchard management are included and
EPA ratings of “highly toxic”, “moderately toxic”, or “practically non-toxic” are noted by color coding in
Table 2. In addition information on synergies, sublethal effects and effects on bee species other than
honey bees are noted in the last column. Growers can easily compare the toxicity ratings of various
pesticides to help them choose a product that is effective against target pests but poses minimal risk to
bees. The Pollinator Network @ Cornell will update this guide as new research becomes available. This
guide is intended to be a companion to the Cornell Pest Management Guide for Commercial Tree Fruit
Production.
Mining bee
Honey bee
Cellophane bee ©
C K
itch
en
©K
L
©K
L
2
How to use this guide This guide consists of a series of tables that summarize all the known products and their associated
active ingredients used in orchard production. It also includes miticides that are used by beekeepers in
New York. Growers and applicators can most effectively use this guide by following three steps:
1. Locate specific pesticide products in Table 1 to determine the product’s active ingredients.
2. Go to Table 2 to find active ingredient toxicity ratings and known synergisms.
3. When possible, choose to apply products that are effective on target pests but least toxic to
bees and do not synergize with other products used.
Table 1: Product formulations and their active ingredients lists
most but not all registered tree fruit pesticides alphabetically by
product name so it’s easy to find the associated active ingredient.
If a product name is not in this product formulation list, please be
aware that the active ingredient is always listed on the product
label. Information on toxicity and synergy is organized by active
ingredient in Table 2.
Table 2: Synergies and acute, chronic, and sublethal toxicities for honey bees and other pollinators
lists all the active ingredients alphabetically, noting EPA honey bee acute toxicity ratings, ability to
synergize, and sublethal effects or impacts to non-honey bee pollinators. Pesticides are grouped
according to class: A) fungicides, antibiotics, and inert ingredients, and B) insecticides (including insect
growth regulators) and adjuvants. In the 3rd to 5th columns of Table 2, the EPA’s acute toxicity ratings
for adult honey bees are reported, and the symbol is added if a synergy has been documented.
Notes on the active ingredients that cause synergistic interactions, as well as information on sublethal
impacts or impacts to other bee species are outlined in the 6th column. Timing of spray is typically noted
on the label, and we encourage applicators to use the most conservative timing when a potentially
synergistic combination must be used.
While this guide has highlighted all laboratory and field
experiments that have measured synergies beween
active ingredients, and the sublethal, chronic, and
developmental impacts of pesticides to honey bees (Apis
mellifera) and other bee species, it is not an exhaustive
list of all product formulations or all pesticides used in
agriculture. The toxicity ratings in columns 3-5 of this
guide refer to current registration standards set forth by
the EPA based on acute toxicity of pesticides to adult
honey bees. Where additional considerations for other
bee species, chronic toxicity, sublethal toxicity, or larval or pupal toxicity are known from scientific
literature, we have included these risks in the ‘Pesticide synergies, sublethal effects, and toxicity to
pollinators other than the honey bee’ column in Table 2.
©Emma Mullen
Bombus impatiens on a cherry flower.
©C Kitchen
3
Understanding the terms in this guide Pesticide toxicity (i.e. acute toxicity) Acute toxicity is the dose or concentration of an active ingredient that it takes to kill 50% of bees that
come into contact with it within 48 hours. The lethal dose of an ingredient is referred to as the LD50
value. Acute pesticide toxicity is grouped into three categories:
highly toxic (LD50 < 2 μg/bee), moderately toxic (LD50 2 - 10.99 μg/bee) practically non-toxic (LD50 > 11 μg/bee)
The EPA is currently working to adjust their registration standards to address risk, which consolidates
toxicity data with exposure predicted from field application rates. These risk rankings will be available
in a few years and, when they are, will be included or referenced in a future edition of this guide.
Synergistic Interactions Traditionally, pesticide toxicity evaluates one active ingredient at a time. With our growing
understanding of the multitude of pesticides bees come into contact with simultaneously,
we now know that to understand the overall risk posed to bees in the environment, we
need to measure how mixtures of pesticides interact with one another. Some pesticides commonly
used in orchard management have been identified as synergists (see Table 2). Certain classes of
fungicides and adjuvants are commonly reported to synergize with insecticides to create greater than
expected effects on bees. For instance, the combination of DMI fungicides (e.g. myclobutanil,
difenoconazole, propiconazole) with some pyrethroids or neonicotinoids have been found to create
these effects. This guide highlights active ingredients that are known synergists and the mixtures that
should be avoided whenever possible to mitigate risk to bees. This information is especially helpful
when planning tank mixes and spray regimes. Keep in mind that the conditions for synergy can vary
depending on formulation, weather, and time since application of an active ingredient. While we
understand that tank mixing is a cost-effective and time-saving practice, we encourage pesticide
applicators to identify and avoid certain pesticide combinations that are likely to cause synergisms,
noted in Table 2.
Systemic Pesticides
“Systemic” pesticides are
able to protect the entire
plant instead of one isolated
part of the plant. The
pesticide is translocated
within the plant from the
point of soil uptake to the
petals, leaves, stem, roots, pollen and nectar to protect the plant from a variety of pests. Unfortunately,
this also means that these pesticides can be present in pollen, nectar, and guttation droplets for days
or weeks, which can result in exposure to pollinators. The most common systemic pesticides are the
The life cycle of a solitary ground nesting bee. Bees can be exposed to
pesticides in soil and in the pollen and nectar they consume as larvae.
Photos by Laura Russo.
4
neonicotinoids (acetamiprid, clothianidin, dinotefuran, imidacloprid, nitenpyram, thiacloprid,
thiamethoxam) and fipronil, a phenylpyrazole insecticide. A real conundrum we face is that some
systemics are only in NY because they are seed coatings on other crops planted in other fields that bees
forage in at the same time as apple bloom, increasing the potential for synergy. Applicators often need
to spray fungicides on plants treated with systemics increasing the potential for synergy when bees
forage. Some neonicotinoids can persist in the soil for years and be taken up by nearby plants at any
time creating a high likelihood for bee exposure and potential to synergize with other pesticides.
Adjuvants and/or inert ingredients Adjuvants are chemicals added to a pesticide spray mix to improve performance. Inert ingredients are
chemicals in a pesticide product formulation aside from the active ingredient(s) . The literature on this
topic is young, so we have included only a handful of these chemicals in Table 2 because recent findings
have demonstrated that they are highly toxic to bees (for example, N-methyl-2-pyrrolidone and
organosilicones).
Tying it all together: adopting an Integrated Pest and Pollinator Management (IPPM) approach to protect pollinators Growers and pesticide applicators have
already made marked adjustments for the
protection of bees by following pesticide
label guidelines. Pesticide labels inform
users about bee precautions in a “Bee
Advisory Box”, in the “Directions for Use”
section, and/or in the “Environmental
Hazards Statement” section of the product
label. These precautions include
information about the time, temperature,
and wind speeds under which pesticides
can be safely applied, and may specify
additional requirements for reducing drift.
Whether growers work closely with a
county extension educator, a crop
consultant, or a distributor, they must
always read the pesticide label carefully.
When reading the label, always note the crops for which the pesticide is registered, the proper mixing
rate, the proper method of application, and the proper timing (e.g., weather conditions, time of day,
stage of bloom) for minimizing negative impacts on non-target organisms and humans. Take note of the
active ingredient name(s). Also note the compatibility of the pesticide with other products that will be
applied at the same time or in the same tank mix. Applicators should verify that the product is currently
Spraying in low-wind conditions can reduce drift, especially
when using a typical airblast sprayer.
©van Dyke
5
registered in their region of New York by searching the products listed in the New York State Pesticide
Administration Database (NYSPAD): http://www.dec.ny.gov/nyspad/. If applicators are using this guide
in another state, they should check their state’s pesticide registration database or the National Pesticide
Information Retrieval System (NPIRS) to determine which pesticides are registered for their use:
http://npirspublic.ceris.purdue.edu/state/.
An integrated pest and pollinator management approach requires growers to be aware of their pest
populations through scouting early and often, to use non-chemical methods to delay the need for
chemical applications, and when pesticides are warranted, to choose products that are effective and
pose the lowest risk to bees and other non-target organisms.
IPPM: Putting the “Pollinator” in IPM: 1) Read the entire product label to find pollinator protection
guidelines during application, and follow label directions.
2) Select pesticides that are effective against target pests, but least
toxic to bees.
3) Avoid using pesticides or tank mixing pesticides and adjuvants that
are noted in this guide to synergize with each other.
4) Choose sprayer nozzles and settings that reduce drift. Follow label
directions regarding wind speed and temperature inversions to
avoid drift to areas of potential bee habitat at field edges.
5) Unless the product label notes otherwise, avoid applying
insecticides when high humidity at low temperatures are forecast
following application. Dew is common under these conditions, which
allows residues to remain toxic up to twice as long.
6) Prevent bees from visiting the orchard floor while pesticides are being applied by frequently mowing
broadleaf weeds (e.g., dandelions). Leaving flowers on the orchard floor can expose bees to
pesticides.
7) Follow label directions to reduce
contamination of surface waters (e.g.,
irrigation ditches, retention ponds,
creeks, etc). Bees actively collect water
and mud from these sources.
8) Develop a communication strategy to
alert nearby beekeepers at least 24
hours in advance of applying a highly
toxic pesticide. Consider using a written
pollination contract with beekeepers
who provide pollination services to
discuss an IPPM plan in advance. An
example template can be found in Appendix A of this guide.
Bees visit plants, like this willow,
in field edges even when a crop is
not in bloom
Mowing dandelions and other flowering weeds in orchard
lanes can protect bees from pesticides exposure.
©van Dyke
©McArt
6
Fungicides, antibiotics and inert ingredients Abamectin (ingredient in)
N-methyl -2-pyrrolidone (NMP)
Abound azoxystrobin Academy difenoconazole +
fludioxonil Acadia azoxystrobin Actigard acibenzolar-s-methyl Aframe azoxystrobin Agricure potassium bicarbonate Agri-mycin streptomycin AgriTin* triphenyltin hydroxide* Alamo propiconazole Aliette fosetyl-al Alsa* propiconazole Amistar difenoconazole Aprovia benzovindiflupyr AproviaTop benzovindiflupyr +
di fenoconazole Ardent (ingredient in)
N-methyl -2-pyrrolidone (NMP)
Azoxystar azoxystrobin Badge SC & X2§ copper oxychloride +
copper hydroxide Banner Maxx propiconazole Biocover mineral oil Bonide complete fruit tree spray
captan
Bonide Fruit Tree & Plant Guard
boscalid+pyraclostrobin+ lambda-cyhalothrin
Bordeaux§ copper sulfate BravoUltrex chlorothalonil Bromazil imazalil Bumper 250 EC* propiconazole BVA mineral oil C.O.C.S. copper oxychloride +
copper sulfate Cabrio EG pyraclostrobin Camelot O§ copper octanoate Cannonball fludioxonil Captan 50 WP captan Captan 80 WDG captan Captec 4L captan CaptEvate fenhexamid + captan Catamaran chlorothalonil + potassium
phosphite Cease§ Bacillus subtilis Champ§ copper hydroxide Cherokee propiconazole Civitas Turf mineral oil Contans Coniothyrium minitans Crystalline BASF* products
pyraclostrobin
Cueva§ copper octanoate Cuprofix Ultra§ copper sulfate Cuproxat§ copper sulfate Curzate 60 DF cymoxanil Damoil mineral oil Decco Pyr. 400 SC pyrimethanil Deccozil imazalil Decree fenhexamid Dithane mancozeb Double Nickel§ Bacillus amyloliquefaciens Echo 90 DF & Lite chlorothalonil Eclipse Turf iprodione
EFOG-160-PYR storage pyrimethanil Elatus benzovindiflupyr Elevate fenhexamid Empress Intrinsic pyraclostrobin Encartis boscalid + chlorothalonil Endura boscalid Equus products chlorothalonil Ethos§ Bacillus amyloliquefaciens Exilis plus N-methyl -2-pyrrolidone Exponent piperonyl butoxide Ferbam ferbam Fireline oxytetracycl ine Firewall s treptomycin Flint tri floxystrobin Flint Extra tri floxystrobin Fontelis penthiopyrad Fortix flutriafol Fortuna mancozeb Freshgard imazalil Fungaflor imazalil Fungazil imazalil Fungisol debacarb Gem 500 SC tri floxystrobin Glacial Spray mineral oil Heritage azoxystrobin Incognito 4.5F thiophanate-methyl Indar2F fenbuconazole Initiate chlorothalonil InspireSuper difenoconazole + cyprodinil Iprodione2F Select* iprodione Kaligreen potassium bicarbonate Kasumin 2L kasugamycin Kestrel Mex* propiconazole Kocide§ copper hydroxide Kodiak§ Bacillus subtilis Liquid Copper Products§
copper octanoate
Luna Sensation† fluopyram + tri floxystrobin Luna Tranquility† fluopyram + pyrimethanil ManKocide mancozeb + copper
hydroxide Mantis propiconazole Manzate Flowable* mancozeb Manzate Max T&O mancozeb Manzate ProStick mancozeb Marazo propiconazole Mastercop§ copper sulfate Menara propiconazole Merivon Xemium*† fluxapyroxad +
pyraclostrobin Meteor* iprodione MilStop potassium bicarbonate MoncoatMZ flutolanil + mancozeb Monterey§ Bacillus amyloliquefaciens Mural benzovindiflupyr MycoShield oxytetracycl ine Natria§ Bacillus subtilis Nevado* iprodione Omni mineral oil Oreon PCNB (quintozene or
pentachloronitrobenzene) Ortho Elements Garden§
copper octanoate
PBO-8 piperonyl butoxide Penbotec 400 SC pyrimethanil Penncozeb mancozeb
Polyram 80 DF metiram Presidio* fluopicolide Pristine fungicide boscalid + pyraclostrobin Procure* tri flumizole* Propi Max propiconazole Pure Spray mineral oil Quadris Ridomil Gold SL
azoxystrobin + mefenoxam
Quadris F azoxystrobin Quadris Opti azoxystrobin +
chlorothalonil Quadris Top azoxystrobin +
di fenoconazole Quali-Pro mefenoxam Quash metconazole Quilt azoxystrobin +
propiconazole QuiltXcel azoxystrobin +
propiconazole Quintec quinoxyfen Rally 40 WSP myclobutanil Ranman 400SC cyazofamid Regalia reynoutria Revitalize§ Bacillus amyloliquefaciens Rhyme flutriafol Rovral 4 F* iprodione Scala pyrimethanil Scholar fludioxonil Serenade§ Bacillus subtilis Sonata§ Bacillus subtilis Sonoma 20 EW AG myclobutanil Sonoma 40 WSP myclobutanil Sovran kresoxim-methyl Streptrol streptomycin SubdueGR mefenoxam- nonbearing Sulfur sul fur SuperTin* triphenyltin hydroxide* Syllit FL dodine Tartan tri floxystrobin Temprano (ingredient in)
N-methyl -2-pyrrolidone (NMP)
Terraguard* tri flumizole* Tilt propiconazole Topguard† flutriafol Topguard EQ† azoxystrobin+flutriafol Topsin M thiophanate-methyl Tourney metconazole Triathlon§ Bacillus amyloliquefaciens Ultra Flourish mefenoxam Vanguard WG cyprodinil Vault§ Bacillus amyloliquefaciens Velum Prime*† fluopyram Vivando metrafenone Warden RTA mefenoxam + fludioxanil Ziram zi ram Zoro (ingredient in) N-methyl -2-pyrrolidone
(NMP)
Products with insecticide and fungicide mixtures Adage ST thiamethoxan + fludioxonil
+ mefenoxam Bonide fruit tree & plant guard
boscalid + pyraclostrobin + lambda-cyhalothrin
Cruiser Maxx thiamethoxan + fludioxonil + mefenoxam
Table 1. Product formulations and their active ingredients Product Name Active ingredient Product Name Active ingredient Product Name Active ingredient
7
Insecticides, Insect growth regulators and adjuvants Abamex abamectin Aceto*† bifenthrin Acramite bifenazate Actara*† thiamethoxam Activator90 polyethoxylated
nonylphenol (N-90) Admire Pro* imidacloprid Advise 4* imidacloprid Agree WG§ Bacillus thuringiensis Agri-Flex*† abamectin +
thiamethoxam Agri-Mek* abamectin Altacor*† chlorantraniliprole Ammo cypermethrin Annihilate* methomyl Apistan tau-fluva linate Apollo clofentezine Applaud IGR buprofezin Aquaflow tau-fluva linate Arvida acetamiprid Asana XL* es fenvalerate Assail acetamiprid Avaunt indoxacarb Aza-Direct§ azadirachtin AzaGuard§ azadirachtin Azatin§ azadirachtin Azomar acetamiprid Banter bifenazate Baythroid XL* beta-cyfluthrin Baythroid* cyfluthrin Beleaf products flonicamid Belt SC*† Flubendiamide Besiege*† chlorantraniliprole +
lambda-cyhalothrin Bifenture* bifenthrin BioBit§ Baci llus thuringiensis
subspecies and proteins Bonideoil§ horticultural oil Brigade 10WSB* bifenthrin Brigade 2EC* bifenthrin Buprofezin 65% WP buprofezin Butacide piperonyl butoxide Calypso 4 Flowable*†
thiacloprid
Carbaryl 4L carbaryl Cease Bacillus subtillis Centaur*† buprofezin Collate* ethephon Companion Bacillus subtillis Confirm*† tebufenozide Corrida 29SL* methomyl Counter Lock-n-Load*
terbufos
Counter 15G Smartbox*
terbufos
Crossfire polyethoxylated nonylphenol (N-90)
Damoil horticultural oil Danitol* fenpropathrin Delegate WG spinetoram Demand SC, EZ & G lambda-cyhalothrin Des-X§ insecticidal soap Diazinon* diazinon Dimethoate* dimethoate Dimilin*† diflubenzuron
DiPel DF§ Baci llus thuringiensis subspecies and proteins
Drexel carbaryl carbaryl Durivo*† thiamethoxam +
chlorantraniliprole Endigo*† thiamethoxam + lambda-
cyhalothrin Entrust SC§ spinosad Envidor*† spirodiclofen Epi-Mek abamectin Esteem pyriproxyfen Exirel*† (Dupont) cyantraniliprole Falgro gibberellic acid Fanfare* bifenthrin Fascination benzyladenine +
gibberellins Flagship*† thiamethoxam Flonicamid 50WG flonicamid Floramite bifenazate Fyfanon malathion GameStop§ kaolin Gaucho 480 imidacloprid Gaucho 600 imidacloprid Gaucho XT imidacloprid GibGro gibberellic acid Gladiator* zeta-cypermethrin +
avermectin Gnatrol§ Bacillus thuringiensis
subspecies and proteins Hero* bifenthrin + piperonyl
butoxide Imidan* phosmet Induce non-ionic surfactant Intrepid*† methoxyfenozide IntruderMax acetamiprid Javelin§ Bacillus thuringiensis
subspecies and proteins JMS Stylet§ horticultural oil Justice acetamiprid Kanemite acequinocyl Kopa§ insecticidal soap Lannate products* methomyl Leverage 360* beta-cyfluthrin +
imidacloprid Leverage 2.7* cyfluthrin + imidacloprid* Leverage products imidacloprid LI-700 non-ionic surfactant Lorsban* chlorpyrifos M1-LV* methomyl Macho 2 & 4 imidacloprid Magister fenazaquin Magus fenazaquin Mavrik tau-fluva linate Molt-X§ azadirachtin Movento* spirotetramat M-pede§ insecticidal soap Mustang & Mustang MAXX*
piperonyl butoxide & zeta-cypermethrin
N-90 polyethoxylated nonylphenol (N-90)
Nealta cyflumetofen Neemix§ azadirachtin Nexter† pyridaben N-Large gibberellic acid Novagib gibberellic acid Nudrin* methomyl NuFarm Abamectin abamectin Omni acetamiprid Onager hexythiazox
Pedestal* novaluron Perimeter tau-fluva linate Perlan benzyladenine +
gibberellins Phase organosilicone surfactant Platinum 75 SG*† thiamethoxam Portal fenpyroximate Pounce 25 WP* permethrin Proclaim* emamectin benzoate Pro-Gibb gibberellic acid ProGibb 4% gibberellic acid Promalin benzyladenine +
gibberellins Provide 10% SG gibberellic acid Provoke* imidacloprid Pure Spray§ horticultural oil Pybuthrin piperonyl butoxide Pycana pyrethrin PyGanic§ pyrethrin Pyrenone pyrethrin Radiant SC spinetoram Regent fipronil Regulaid non-ionic surfactant Return*† oxamyl Rimon* novaluron Safer§ Bacillus thuringiensis
subspecies and proteins Safer§ insecticidal soap Savey hexythiazox Seduce Insect Bait§ spinosad Serenade Bacillus subtillis Sevin carbaryl ShuttleO acequinocyl Silencer* lambda-cyhalothrin Silicone organosilicone surfactant Silkin organosilicone surfactant Silt organosilicone surfactant SpinTor 2SC§ spinosad Spirotetramat 240SC*
spirotetramat
Steward indoxacarb Subtilex NG Bacillus subtillis SuffOil-X§ horticultural oil Sultrus* beta-cyfluthrin Sunspray horticultural oil Supracide methidathion Surround 95 WP§ kaolin Talus 70DF*† buprofezin Thuricide§ Bacillus thuringiensis
subspecies and proteins Tombstone* cyfluthrin Tourismo*† flubendiamide Triact 70§ azadirachtin Trilogy§ azadirachtin Tundra* bifenthrin Typy benzyladenine +
gibberellins Ultra-Fine horticultural oil Vendex* fenbutatin-oxide Ventas*† oxamyl Verve* ethephon Voliam Flexi*† thiamethoxam +
chlorantraniliprole Warrior II Zeon*†∆ lambda-cyhalothrin Xentari§ Baci llus thuringiensis
subspecies and proteins Zeal etoxazole ZetaGuard LBT zeta-cypermethrin + PBO Zoro abamectin
Product Name Active ingredient Product Name Active ingredient Product Name Active ingredient
8
Table 2. Pesticide synergies and acute, chronic, and sublethal toxicities for honey bees and other pollinators
Key to table abbreviation, symbols, and colors
- Restricted-use pesticide
- Not for use in Nassau and Suffolk counties of New York
- Meets USDA organic standards
- Identifies a chemical that at least one study has shown synergy with other active ingredients or products.
- Identifies a formulation containing more than one active ingredient, at least one of which has been shown to synergize with other chemicals
EPA standard toxicity ratings: acute oral and/or contact toxicity to the honey bee (Apis mellifera)
- Highly toxic (acute LD50 < 2μg/bee)
- Moderately toxic (acute LD50 2 - 10.99μg/bee)
- Practically non-toxic (acute LD50 >11 μg/bee)
Fungicides, antibiotics and inert ingredients Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
acibenzolar-S-methyl
benzothiadiazole [P01]
Actigard
azoxystrobin
QoI-methoxy-acrylate
fungicide [11]
Quadris F,
Abound,
Acadia, Aframe,
Heri tage
The combination of Quadris® (azoxystrobin) and 2SE
Select® (iprodione) produce a low level synergy (still
practically non-toxic) in late season honey bees that
increases with time from application; 60% mortality at
10 days1. No synergy detected with thiacloprid2.
azoxystrobin +
difenoconazole
QoI-methoxy-acrylate +
DMI-triazole fungicide [11+3]
Quadris Top
See azoxystrobin and difenoconazole separately for
synergy information.
azoxystrobin + flutriafol
QoI-methoxy-acrylate +
DMI-triazole fungicide [11+3]
TopguardEQ
azoxystrobin +
propiconazole
QoI-methoxy-acrylate +
DMI-triazole fungicides [11+3]
Qui l t, Quilt
Xcel
See azoxystrobin and propiconazole separately for
synergy information.
9
Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
Bacillus amyloliquefaciens
Microbial disruptor of
pathogen produced by natural
bacterium [44]
Double Nickel§,
Ethos§,
Monterey§,
Revi talize§,
Triathlon§,
Vault§
Bacillus subtilis
Microbial disruptor of
pathogen, toxin produced by
natural bacterium [44]
Cease§,
Kodiak§, Natria§,
Serenade§,
Sonata§, etc.
The wet application of B. subtilis strain QST713
(Serenade®) reduced honey bee brood production and
was highly toxic to the bumble bee (Bombus terrestris)3.
Tests on the dry application of B. subtilis strain QST713
(Serenade®) and strain QRD132 (Serenade®) did not
significantly impact Bombus impatiens4 or honey bees5.
benzovindiflupyr
SDHI-pyrazole-4-carboxamide
fungicide [7]
Aprovia *,
Elatus*,
Mural* A new product for bitterrot.
boscalid
SDHI-pyridine-carboxamide
fungicide [7]
Endura
(grape)
Synergizes with clothianidin and thiamethoxam6.
boscalid + pyraclostrobin
SDHI-pyridine-carboxamide +
QoI- methoxy-carboxamide
fungicides [7+11]
Coronet,
Pris tine
Pristine® (boscalid+pyraclostrobin) synergizes with
chlorpyrifos7 reducing queen emergence, with Iprodione
2SE Select® (iprodione) increasing honey bee mortality1,
and with Rovral® (iprodione) negatively impacting
solitary bee species nesting behavior8.
captan
phthalimide fungicide [M4]
Captan 50
WP, Captan,
80 WDG, Captec 4L
Studies have found captan to increase honey bee brood
mortality to a moderately toxic level9,10 and alter larval
feeding capacity11. A study conducted by the USDA Bee
Lab in Weslaco, TX found that the inert ingredients
mixed with captan make it highly toxic12. Other
laboratory studies report captan to be highly toxic to
mason bees13 and leafcutter bees 14,15 but practically
non-toxic to bumble bees at recommended field rates 16.
chlorothalonil
chloronitrile fungicide [M5]
Bravo ZN,
Bravo Ultrex,
Echo
Products ,
Equus, Initiate
Synergizes with alpha-cypermethrin and lambda-
cyhalothrin17 and the beekeeping miticides tau-
fluvalinate, coumaphos 18,19, and thymol18. Also
synergizes with Cerconil® (thiophanate-methyl).
Chlorothalonil exhibits cumulative oral toxicity in honey
bee larvae reared on field relevant doses for 6 days 19 and
increases honey bee and bumble bee susceptibility to
Nosema infection20,21 and entombed pollen inside the
honey bee hive20.
copper hydroxide
inorganic
fungicide/bacteriacide [M1]
Kocide§,
Champ§
10
Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
copper octanoate
inorganic
fungicide/bacteriacide [M1]
Camelot O§, Cueva§,
Liquid copper
Products§,
Ortho
Elements
Garden§
copper oxychloride/
copper hydroxide
inorganic
fungicide/bacteriacide [M1]
Badge SC &
X2§
Copper oxychloride synergizes with imidacloprid22.
copper oxychloride/copper
sulfate
inorganic
fungicide/bacteriacide [M1]
C.O.C.S.
Copper oxychloride synergizes with imidacloprid22.
copper sulfate
inorganic
fungicide/bacteriacide [M1]
Bordeaux§,
Cuprofix Ultra§,
Cuproxat§,
Mastercop§
Highly toxic to a stingless bee species via oral exposure23.
cyprodinil
anilino-pyrimidine fungicide,
[9]
Vanguard WG
Moderate toxicity when it synergizes with thiacloprid2.
difenoconazole
DMI-triazole fungicide [3]
Quadris-Top,
Amistar, etc.
Synergizes with deltamethrin24 and the tau-fluvalinate25
product Mavrik® inducing hypothermia in honey bees.
difenoconazole +
fludioxonil
DMI-triazole + phenylpyrroles
fungicides [3+12]
Academy
See difenoconazole and fludioxonil separately for
synergy information.
difenoconazole + cyprodinil
DMI-triazole + anilino-
pyrimidine fungicides [3+9]
Inspire Super
See difenoconazole and cyprodinil separately for synergy
information.
dodine
guanidine fungicide [U12]
Syl l it FL
fenbuconazole
DMI-triazole fungicide [3]
Indar 2F
Synergizes with tau-fluvalinate18 making it highly toxic to
honey bees. At a field relevant dose Indar 2F®
(fenbuconazole) synergizes with acetamiprid26 in a
solitary bee, doubling the toxicity of acetamiprid, making
it borderline highly toxic (LD50 2.1).
11
Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity Practically
non-toxic Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
fenhexamid
SBI-KRI hydroxyanilide
fungicide [17]
Decree,
Elevate
fenhexamid + captan
SBI-KRI hydroxyanilides +
phthalimide [17+M4]
CaptEvate
See captan separately for toxicity notes.
ferbam
dithiocarbamate fungicide
[M3]
Ferbam granuflo
fludioxonil
phenylpyrroles fungicide [12]
Cannonball,
Scholar
Impacts honey bee learning behavior27.
fluopicolide
acylpicolide fungicide [U]
Pres idio* for
landscape
fruit trees
fluopyram
pyridinyl-ethyl-benzamide
fungicide [7]
Velum
Prime*†,
Broadform*†
fluopyram + pyrimethanil
Pyridinyl-ethyl-benzamide +
anilino-pyrimidine fungicides
[7+9]
Luna
Tranquility*†
flutriafol
DMI-triazole fungicide [3]
Rhyme†
Synergizes with lambda-cyhalothrin28,29 making lambda-
cyhalothring 3 times more toxic. Although EPA classifies
this pesticide as low toxicity to honey bees, the
European Food Safety Authority has determined it
exhibits moderate toxicity when the a.i. is consumed by
bees30.
fluxapyroxad +
pyraclostrobin
SDHI-pyrazole-4-carboxamide
+ methoxy-carboxamide
fungicides [7+11]
Merivon
Xemium*†
See pyraclostrobin separately for synergy information.
fosetyl-Al
Aluminum tris (O-
ethylphosphonate) fungicide
[P07(33)]
Al iette WDG
12
Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
imazalil
DMI-imidazole fungicide [3]
Fungaflor, Freshgard,
Fungazil Synergizes with cypermethrin, fipronil , and
thiamethoxam in bumble bees 31 and lambda-cyhalothrin
in honey bees29.
iprodione
dicarboxamide fungicide [2]
Meteor*,
26GT*,
Nevado*, Rovra l 4 F*,
Iprodione 2F
Select*
Synergizes with Pristine® (pyraclostrobin+ boscalid)8.
Compass SC® (iprodione + thiophanate methyl), was
found to synergize with the varroacide, Mavrik® (tau-
fluvalinate)32 and decrease the repellency of honey bees
to cypermethrin17 thereby increasing their exposure.
The combination of Iprodione 2SE Select® (iprodione)
and Quadris® (azoxystrobin) produce a low level synergy
(still practically non-toxic) in late season honey bees that
increases with time from application; 60% mortality at
10 days1. One study reports high toxicity to honey bee
larvae10 and another study reports sublethal effects on
some solitary bees8.
kasugamycin
antibiotic [24]
Kasumin 2L
kresoxim-methyl
QoI-oximino-acetate fungicide
[11]
Sovran*†
mandipropamid +
difenoconazole
CAA mandelic acid amides +
DMI- triazole fungicides
[40+3]
Revus Top
See difenoconazole separately for synergy information.
mancozeb
dithiocarbamate fungicide
[M3]
Dithane*, Kovera ll*,
Manzate,
Penncozeb*
When combined with alpha-cypermethrin or lambda-
cyhalothrin studies found a 2-4 fold decrease in the
contact toxicities17 of these two insecticides. Synergy not
detected with thiacloprid2.
mancozeb + copper
hydroxide dithiocarbamate
fungicide + inorganic
fungicide/bactericide
[M3+M1]
ManKocide*
See mancozeb separately for synergy information.
mefenoxam (metalaxyl-M)
phenylamide acylalanine
insect growth regulator [4]
Qual i-Pro
Mefenoxam,
Ultra Flourish
metconazole
DMI- triazole[3]
Quash,
Tourney
Synergy with tau-fluvalinate18 causing a 3-4 fold increase
in contact toxicity of this miticide.
13
Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
metiram
dithiocarbamate fungicide
[M3]
Polyram 80DF
metrafenone
benzophenone fungicide [50]
Vivando
myclobutanil
DMI-triazole fungicide [3]
Ral ly 40 WSP,
Sonoma 20
EW AG,
Sonoma 40
WSP
Synergizes with clothianidin, imidacloprid,
thiamethoxam33, lambda-cyahalothrin29,34, tau-
fluvalinate18 via oral and/or contact exposure in honey
bees. Synergy with lambda-cyhalothrin also affects
bumble bees feeding on pollen34. Synergy is not detected
with thiacloprid33.
mineral oil
Horticultural Spray
Biocover,
BVA, Damoil,
Civi tas Turf,
Glacial Spray,
PureSpray, Omni
N-methyl-2-pyrrolidone
(NMP)
inert ingredient often used in
pesticide formulations as a co-
solvent
NMP is in
abamectin
0.15EC,
Ardent 0.15, Exi l is plus,
Temprano,
Zoro
This inert ingredient is highly toxic to honey bee larvae19.
oxytetracycline
tetracycline antibiotic
Fireline,
MycoShield One study found a synergy with tau-fluvalinate35 while
another study did not show synergy with tau-
fluvalinate18.
penthiopyrad
pyrazole-4-carboxamide
fungicide [7]
Fontelis
piperonyl butoxide
synergist
Exponent,
PBO-8, and
various pyrethrum
products
Synergizes with acetamiprid36, coumaphos37,18,
cyfluthrin38, fenpyroximate18, lambda-cyhalothrin28,38,
permethrin39, tau-fluvalinate37,18, and thiacloprid36 as
well as imidacloprid (a.i.) and the imidacloprid
formulation Advise®36,40.
potassium bicarbonate
Inorganic salt
Agricure,
Ka l igreen,
Mi lStop
14
Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
propiconazole
DMI-triazole fungicide [3]
Alamo*, Alsa*, Propi
Max, Bumper
250EC*,
Cherokee,
Kestrel Mex*,
Menara,
Marazo, Tilt,
Mantis,
Banner Maxx
Synergizes with alpha-cypermethrin29, acetamiprid,
imidacloprid, thiacloprid36,33, lambda-cyhalothrin29,17,
tau-fluvalinate18, thiamethoxam33 and clothianidin in
honey bees. One study determined that propiconazole
reduced the toxicity of thiacloprid33. Also synergizes with
clothianidin in bumble bees and some solitary bees 41
however another study demonstrated only additive
effects of clothianidin42. Propiconazole alone decreases
bumble bee reproduction43.
pyraclostrobin
QoI-methoxy-carboxamide
fungicide [11]
Crysta l line
BASF*
products,
Cabrio EG,
Empress
Intrinsic
Synergizes with fenpyroximate and the beekeeping
miticide tau-fluvalinate18. Pristine® (pyraclostrobin +
boscalid) synergizes 2SE Select® (Iprodione)1 and
negatively impacts nesting success of some solitary bees8
and reproductive success 44 and immunity in honey bees 7.
When combined with fipronil , honey bee larval feeding
decreases45.
pyrimethanil
anilino-pyrimidine fungicide
[9]
Decco Pyr.
400 SC, Sca la,
Penbotec 400
SC, EFOG-160
quinoxyfen
azanaphthalene
aryloxyquinoline fungicide [13]
Quintec
reynoutria
Botanical extract of
Reynoutria sacchalinensis
Regalia
streptomycin
antibiotic [25]
Agri -mycin*, Streptrol,
Fi rewall
sulfur
inorganic natural element
[M2]
Sul fur, Some products §
Moderate oral toxicity can remain up to 7 days 46.
thiophanate-methyl
thiophanate fungicide [1]
Tops in M,
Incognito 4.5F
Synergizes with tau-fluvalinate17,18, flumethrin, and
lambda-cyhalothrin17 becoming highly toxic to honey
bees. Synergizes with product formulations containing
the active ingredients imidacloprid, deltamethrin or
chlorothalonil 47 to become highly toxic to honey bees
and other bees when consumed.
trifloxystrobin
methoxy-carboxamide
fungicide [11]
Fl int, Flint
Extra , Gem
500SC,
15
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
triflumizole
imidazole fungicide [3]
Procure*, Terraguard*
Synergizes with acetamiprid, imidacloprid, and
thiacloprid36.
ziram
dithio-carbamate fungicide
[M3]
Ziram
Larval mortality in laboratory studies10.
Mixtures of fungicides and insecticides Active Ingredient Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
boscalid + pyraclostrobin + lambda-cyhalothrin SDHI-pyridine-carboxamide + QoI-methoxy-carboxamide fungicides + a pyrethroid
insecticide [7+11+3A]
Bonide Fruit
Tree and
Plant Guard
See boscalid, pyraclostrobin and lambda-cyhalothrin separately for synergy and toxicity information.
thiamethoxam + fludioxonil + mefenoxam nitro-neonicotinoid insecticide
+ phenyl pyrrole + phenyl amide acylalanine fungicides (4A+12+ 4)
Adage ST, Cruiser MAXX See thiamethoxam and mefenoxam separately for
synergy information.
Insecticides (including insect growth regulators) and adjuvants
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
abamectin /avermectin avermectin insecticide [6]
Agri -Mek*,
Abamex, Epi-
Mek*,
NuFarm
abamectin*, Zoro*
Vertimec® (abamectin) formulation which includes
unknown inert ingredients produces a synergistic response that was 709x /1870x more toxic to honey bees and Melipona bees than the active ingredient,
abamectin alone48. Highly toxic both topically and orally to honey bees49 and arrests reproduction in bumble bees50. Other non-honey bee species exhibits moderate to high toxicity via contact and oral exposure,
respectively51.
abamectin + thiamethoxam avermectin
+ nitro-neonicotinoid insecticide [6+4A]
Agri -Flex*†
See abamectin separately for toxicity information and thiamethoxam separately for synergy information.
acequinocyl quinolone insecticide [20B]
Kanemite,
Shuttle O Topical and oral exposure arrests bumble bee reproduction50.
16
Active Ingredient
Chemical group
[Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee
species other than the honey bee
acetamiprid cyano-neonicotinoid
insecticide [4A]
Assail, Arvida, Azomar,
Justice, Omni,
Intruder Max,
Synergizes with piperonyl butoxide (PBO), S,S,S-tributylphosphorotrithioate (DEF), triflumizole36, propiconazole36,34, and Indar2® (fenbuconazole)26 making these highly toxic mixtures. Synergy with
propiconazole34 and Indar2® (fenbuconazole)26 is also present in bumble bees and mason bees respectively.
azadirachtin Naturally occurring tetranortriterpenoid Insect growth regulator [UN]
Aza-Direct§,
AzaGuard§,
Molt-X§,
Neemix§,
Azatin§, Triact
70§, Tri logy§
Oral exposure at field relevant dose causes honey bee larval mortality and sublethal effects on adult body
size52–54. Oral exposure below, at, and above a field relevant does causes bumble bee worker mortality and sublethal effects on reproduction and body mass 55.
Bacillus subtillis Microbial disruptor of insect midgut membranes [11A]
Cease,
Companion, Serenade
(Max, Opti ,
ASO, Soi l),
Subti lex NG
B. subtilis is toxic to bumble bee species (B. terrestris)3 and exhibits sublethal effects on reproduction in Bombus impatiens4.
Bacillus thuringiensis subspecies and proteins Microbial disruptor of insect midgut membranes [11A]
BioBit§, DiPel
DF§,
Gnatrol§,
Javelin§,
Monterey§,
Safer§,
Thuricide§,
Xentari§
Negative sublethal impacts on honey bee physiology56.
benzyladenine + gibberellins Insect growth regulators
Perlan,
Promal in,
Fascination
beta-Cyfluthrin pyrethroid insecticide [3A]
Baythroid
XL*, Sul trus*,
Tempo SC*
The parent chemical, cyfluthrin synergizes with piperonyl
butoxide38 becoming 30 times more toxic to honey bees. It also impacts honey bee behavior38 and is highly toxic topically and orally to bumble bees 34,57
beta-Cyfluthrin + imidacloprid pyrethroid + cyano-neonicotinoid insecticide
[3A+4A]
Leverage
360*
See cyfluthrin and imidacloprid separately for synergy
and toxicity information.
bifenazate Insect growth regulator [20D]
Acramite,
Banter,
Floramite
Moderate and High toxicity, topically and orally, relatively to bumble bees including sublethal effects at just 1/10 - 1/2 MFRC50. Honey bee mortality increased 5-fold, 10 days after exposure58.
17
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
bifenthrin pyrethroid insecticide [3A]
Aceto*†, Bifenture*,
Brigade
WSB*†,
Brigade EC*†,
Fanfare*,
Tundra EC*
Synergizes with the miticide Apistan® (tau-fluvalinate)59. Highly toxic to bumble bees59,34 however bifenthrin residue is typically not frequently found in pollen and nectar34. Pyrethroids in general are well known to
synergize with piperonyl butoxide and triazole fungicides17,29,37,60,61.
bifenthrin + zeta-cypermethrin w/ piperonyl butoxide pyrethroid insecticide +
synergist [3A+synergist]
Hero*
See bifenthrin, zeta-cypermethrin and piperonyl butoxide separately for other synergy information. Piperonyl butoxide is a well known synergist with pyrethroids l ike bifenthrin. Highly toxic to bumble
bees59,34.
buprofezin Insect growth regulator [16]
Applaud
IGR*†,
buprofezin
65% WP*†,
Centaur*†
The product formulation Buprofezin 65% WP® exhibits
moderate toxicity48.
carbaryl carbamate insecticide [1A]
Sevin
Carbaryl ,
Drexel
Carbaryl ,
Carbaryl 4L
Highly toxic to bee species other than the honey bee62. Used as a thinner at petal fall it impacts the bee
community that typically are still visiting petal -less flowers.
chlorantraniliprole anthranilic diamide insecticide
[28]
Altacor*† Suppresses reproduction in worker bumble bees 63. Synergy not detected with propiconazole in honey bees64.
chlorantraniliprole + lambda-cyhalothrin anthranilic diamide + pyrethroid insecticide [28+3A]
Bes iege*†
See chlorantraniliprole and lambda-cyhalothrin
separately for synergy and toxicity information.
chlorpyrifos organophosphate insecticide [1B]
Lorsban*
Synergizes with propiconazole65 doubling the toxicity. When combined with the product formulation Pristine®
(pyraclostrobin + boscalid) it reduces honey bee queen emergence7. Highly toxic to bumble bees66,67,34, solitary bees51 and chronically lethal to honey bee larvae19.
chlorpyrifos + bifenthrin organophosphate + pyrethroid
insecticide [1B+3A]
Tundra
Supreme*†
See bifenthrin and chlorpyrifos separately for synergy
and toxicity information.
clofentezine tetrazine ovicide/miticide, an insect growth inhibitor [10A]
Apol lo
cyantraniliprole anthranilic diamide insecticide [28]
Dupont
Exirel*†
18
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
cyflumetofen beta-ketonitrile miticide [25A]
Nealta
cyfluthrin pyrethroid insecticide [3A]
Baythroid*,
Tombstone*
Synergizes with piperonyl butoxide38 becoming 30 times more toxic to honey bees. It also impacts honey bee
behavior38 and is highly toxic topically and orally to bumble bees34,57
cyfluthrin + imidacloprid pyrethroid +
nitro-neonicotinoid insecticide [3A+4A]
Leverage2.7*,
Leverage
360*
See cyfluthrin and imidacloprid separately for synergy
information.
cypermethrin pyrethroid insecticide [3A]
Ammo, Fastac
Synergizes with imazalil in at least one bumble bee species31. Alpha-cypermethrin, an isomer of
cypermethrin, synergizes with Bravo SC®, 500g/l (chlorothalonil), Tilt EC®, 250g/l (propiconazole), and Sportak EW®, 450 g/l (prochloraz), and increases toxicity of Derosal WG® 80% (carbendazim), Compass SC®
15.5%/15.5% (iprodione + thiophanate methyl) and other triazoles including Folicur EW®, 250 g/l (tebuconazole) and Plover EC®, 250 g/l (difenoconazole)17. Both cypermethrin and zeta-
cypermethrin are highly toxic to solitary bees68. Cypermethrin increases Chronic Paralysis Virus (CPV) infection69.
diazinon organophosphate insecticide [1B]
Diazinon*
Highly toxic to bumble bees and some solitary bees as well as honey bees70,62.
diflubenzuron Insect growth regulator [7C]
Dimilin*† Has shown sublethal effects on larvae and fertil ity of adult honey bees71–76; but see77.
dimethoate organophosphate insecticide [1B]
Drexel
Dimethoate*
Highly toxic to bumble bees and some solitary bees 78,13.
emamectin benzoate avermectin insecticide [6]
Proclaim*∆
esfenvalerate pyrethroid insecticide [3A]
Asana XL*
Highly toxic to bumble bees51,34 and exhibits sublethal
effects on megachilid bees 79.
ethephon Insect growth regulator
Col late*,
Verve*
etoxazole etoxazole insecticide [10B]
Zeal Highly toxic to bumble bees when consumed50,56.
fenazaquin pyridazine insecticide [21A]
Magister,
Magus Low toxicity to bumble bees57
19
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
fenbutatin-oxide organotin insecticide [12B]
Vendex*
fenoxycarb (EXPIRED) Insect growth regulator [7B]
Reduces reproduction and the size of winter honey bee
colonies75.
fenpropathrin pyrethroid insecticide [3A]
Danitol 2.4*†
Highly toxic to bumble bees and some solitary bees80.
fenpyroximate pyridazine insecticide [21A]
Porta l
Synergizes with enzyme inhibitors piperonyl butoxide (PBO) and S,S,S-tributylphosphorotrithioate (DEF), fungicides including prochloraz, pyraclostrobin and beekeeping miticides amitraz18, and oxalic acid making
these mixes highly toxic. And in the cases of the beekeeping miticides tau-fluvalinate and coumaphos 18 borderline high toxicity (LD50 2.04-2.4). Although EPA has
reported that this active ingredient is practically non-toxic, one study measured moderate toxicity to honey bees18.
fipronil phenyl pyrazole fungicide [2B]
Regent
Synergizes with imazalil to be lethal to bumble bees at
24 hrs but the toxicity subsides by 48 hrs 31. fipronil is associated with increased Nosema infection81.
flonicamid flonicamid insecticide [29]
Beleaf 50SG,
Flonicamid
50WG
flubendiamide anthranilic diamide insecticide [28]
Belt SC*†,
Tourismo*†
Moderate toxicity when applied topically to honey bees has been reported in laboratory and semi-field
conditions82. Megachile rotundata83 and Bombus impatiens84 were not impacted by Belt SC® (flubendiamide).
gibberellic acid Insect growth regulator
Falgro,
Novagib,
GibGro, N-Large, Pro-
Gibb 4%§,
Pro-Vide
10%SG
Also used as a supplement in the honey bee diet85.
hexythiazox thiazolidine insecticide [10A]
Hexygon,
Savey, Onager
horticultural oil Damoil,
PureSpray§,
Sunspray,
JMS Stylet§,
SuffOi l-X§,
Ultra -Fine,
Bonide oil§
Products with thymol, menthol, and rosemary can be highly toxic, especially when bees are already stressed86–
89). Bees are temporarily inactivated by direct contact with oil sprays; death may occur90.
20
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
imidacloprid nitro-neonicotinoid insecticide
[4A]
Advise 4*, Admire Pro
Protectant*,
Leverage
products,
Macho 2* &
4*, Provoke*
Synergizes with piperonyl butoxide36,40, propiconazole36, triflumizole36, Advise 2FL® (imidacloprid) synergized with Vydate 3.77 CLV® (oxamyl), Transform 5G® (sulfloxaflor), and Domark ME® (tetraconazole)40. Highly toxic to
bumble bees91. May impact groundnesting bees in general92.
indoxacarb oxadiazine insecticide [22A]
Avaunt
High toxicity even at field-realistic doses82,93.
insecticidal Soap Repellant
M-pede§,
Des -X§,
Kopa§, Safer§
kaolin Repellant
Surround
WP§
lambda-cyhalothrin pyrethroid insecticide [3A]
Demand SC*
& EZ* & G*, Si lencer*,
Warrior I I
with Zeon*
Synergizes with flutriafol 28, imazalil, myclobutanil, propiconazole29, prochloraz28,29,60, and piperonyl butoxide28,38 making them 16x more toxic than when
applied alone. Highly toxic to bumble bees80 and some solitary bees80,94.
malathion organosphosphate insecticide [1B]
Fyfanon Highly toxic to bumble bees and some solitary bees 95.
methidathion organosphosphate insecticide
[1B]
Supracide Realistic field exposure moderately toxic34.
methomyl carbamate insecticide [1A]
Annihilate*,
Corrida
29SL*,
Lannate*, Lannate LV,
M1-LV*,
Nudrin*
Moderately to Highly toxic to bumble bees96,57.
methoxyfenozide diacylhydrazine insecticide [18] an insect growth regulator
Intrepid*† Acute and chronic effects to honey bee larvae and adults over time58.
non-ionic surfactant Regulaid,
LI-700, Induce
novaluron benzoylureas insecticide [15]
Pedestal*,
Rimon* Sublethal impacts on egg and larvae of honey bees97,
some bumble bees92,98 and leafcutter bees92,99.
21
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
organosilicone surfactant adjuvant
Phase, Silt, Si lkin, Silicone
Increases susceptibility of bees to disease, resulting in exponentially increased mortality71,100.
oxamyl carbamate insecticide [1A]
Return*†,
Ventas*†
Vydate 3.7CLV® (oxamyl) synergizes with Advise2FL®
(imidacloprid)40. No effects on bumble bees 56.
permethrin pyrethroid insecticide [3A]
Pounce 25
WP*
Synergizes with piperonyl butoxide39. Highly toxic to bumble bees80,101 and solitary bees80,102.
phosmet organophosphate insecticide [1B]
Imidan* Highly toxic to some solitary bees 80. There are often high residues in pollen samples 34.
piperonyl butoxide (PBO) synergist
Ingredient in
Mustang
MAXX*,
Butacide,
Pybuthrin,
and Ambush
Synergizes with acetamiprid36, coumaphos18, cyfluthrin38, fenpyroximate18, lambda-cyhalothrin28,60, permethrin39,28,37, prochloraz28,60, tau-fluvalinate18,38, and
thiacloprid36 making these highly or more highly toxic than when applied alone. Coumaphos increased to moderate toxicity with piperonyl butoxide. The product Advise® (imidacloprid) increased 5.2 fold in toxicity when
combined with piperonyl butoxide, while the active ingredient imidacloprid alone was just 1.7x more toxic40.
polyethoxylated Nonylphenol (N-90) adjuvant
N-90,
Activator 90,
Cross fire
Sublethal effects on behavior of the honey bee in response to the product Activator-9071 as well as to
managed solitary bee species when used alone and in the case of Grow-More® N-90, in combination with Rovral 4F® (iprodione) and Pristine® (pyraclostrobin +
boscalid) which ultimately decreases reproductive output8.
pyrethrin pyrethrin insecticide [3A]
PyGanic§,
Pycana,
Pyrenone
Synthetic forms synergize with multiple pesticide ingredients. See pyrethroids. Some formulations found
to decrease honey bee body temperature103.
pyridaben pyridazine insecticide [21A]
Nexter†
pyriproxyfen Insect growth regulator [7C]
Esteem Exhibits sublethal impacts on honey bee larvae, adult behavior, and survival58,104 as well as bumble bee larvae105.
spinetoram spynosin insecticide [5]
Delegate WG, Radiant SC
spinosad spynosin insecticide [5]
Entrust SC§,
Seduce§,
SpinTor 2SC§,
Conserve SC
Turf Ornamental
Moderate contact and high oral acute toxicity to bumble
bees106,92 as well as sublethal foraging effects 107 on bumble bees. One non-Apis bee species experienced moderate contact toxicity92 while three other species experienced high contact toxicity92,108,23.
22
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
spirodiclofen tetronic acid insecticide [23]
Envidor*† Although EPA classifies spirodiclofen as low toxicity, one study finds moderate toxicity to adult honey bees 109. Chronic exposure s ignificantly reduced honey bee110 and bumble bee reproduction and colony strength50.
spirotetramat tetramic acid insecticide [23]
Movento*,
Spirotetramat
240 SC*
Moderate acute toxicity and high chronic oral toxicity and sublethal reproductive effects to bumble bees 111,4. Moderately toxic to honey bee larvae in laboratory studies with does above field recommendations 112.
tau-fluvalinate (beekeeping) pyrethroid insecticide [3A] a beekeeping miticide.
Apistan, Aquaflow,
Perimeter,
Mavrik
Synergizes with boscalid18, chlorothalonil19,18, fenbuconazole, metconazole, myclobutanil , prochloraz, propiconazole18, piperonyl butoxide38,18 as well as beekeeping miticides coumaphos37,18, thymol, amitraz,
fenpyroximate, and oxalic acid18. Highly toxic to honey bee larvae19. One study on Mavrik® (tau-fluvalinate) and the product ERIA® (difenoconazole+ carbendazim)
resulted in no lethal or sublethal effects on bees25.
tebufenozide Insect growth regulator [7c]
Confi rm*†
Exhibits sublethal effects on honey bee behavior and learning74,71.
thiacloprid *This product is
suspended, please dispose.
cyano-neonicotinoid
insecticide [4A]
Calypso 4
Flowable*†
Synergizes with cyprodinil2, piperonyl butoxide36,
triflumizole and propiconazole39,noted in 29 and is associated with increased Nosema infection in honey bees81. However, one study found no synergy when mixed with tebuconazole, propiconazole or
myclobutanil33. Field relevant exposure is lethal to bumble bee colonies113.
thiamethoxam nitro-neonicotinoid insecticide
[4A]
Actara*†,
Flagship*†,
Platinum 75
SG*†, Cruiser
FS
Synergizes with boscalid6, propiconazole32,33,
myclobutanil33, and tebuconazole33. Synergizes with imazalil in both honey bees and bumble bees 31. Highly toxic to bumble bees114,115 and some solitary bees 116. Synergistic effect on honeybee mortality when co-
exposed to thiamethoxam and Chronic Bee Paralysis Virus117.
thiamethoxam + chlorantraniliprole nitro-neonicotinoid + anthranilic diamide insecticide
[4A+28]
Vol iam
Flexi*†,
Durivo*†
See thiamethoxam and chlorantraniliprole separately for synergy and toxicity information.
thiamethoxam + lambda-cyhalothrin nitro-neonicotinoid +
pyrethroid insecticide [4A+3A]
Endigo*†
See thiamethoxam and lambda-cyhalothrin separately
for synergy information.
23
Active Ingredient Chemical group [Resistance code]
New York
Trade Name
Examples
High
toxicity
Moderate
toxicity
Practically
non-toxic
Synergies, sublethal effects, and toxicity to bee species other than the honey bee
zeta-cypermethrin pyrethroid insecticide [3A]
Mustang MAXX*
See cypermethrin separately for synergy information. Zeta-cypermethrin is highly toxic to solitary bees68.
zeta-cypermethrin + avermectin pyrethroid + avermectin insecticides [3+6]
Gladiator*
See (zeta)-cypermethrin and avermectin separately for synergy and toxicity information.
Literature Cited1. Fisher, A., Coleman, C., Hoffmann, C., Fri tz, B. & Rangel, J. The
synergistic effects of almond protection fungicides on honey bee (Hymenoptera: Apidae) forager survival. J Econ Entomol 110, 802–808 (2017).
2. Schmuck, R., Stadler, T. & Schmidt, H.-W. Field relevance of a
synergistic effect observed in the laboratory between an EBI fungicide and a chloronicotinyl insecticide in the honeybee (Apis mel lifera L, Hymenoptera). Pest Management Science: formerly Pesticide Science 59, 279–286 (2003).
3. Mommaerts, V., Sterk, G., Hoffmann, L. & Smagghe, G. A laboratory eva luation to determine the compatibility of microbiological control agents with the pollinator Bombus terrestris. Pest Management
Science: formerly Pesticide Science 65, 949–955 (2009). 4. Ramanaidu, K. & Cutler, G. C. Di fferent toxic and hormetic responses
of Bombus impatiens to Beauveria bassiana, Bacillus subtilis and spirotetramat. Pest management science 69, 949–954 (2013).
5. Dedej, S., Delaplane, K. S. & Scherm, H. Effectiveness of honey bees in
del ivering the biocontrol agent Bacillus subtilis to blueberry flowers to suppress mummy berry disease. Biological Control 31, 422–427 (2004).
6. Tsvetkov, N. et al. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science 356, 1395–1397 (2017).
7. DeGrandi-Hoffman, G., Chen, Y. & Simonds, R. The effects of
pesticides on queen rearing and vi rus ti ters in honey bees (Apis mellifera L.). Insects 4, 71–89 (2013).
8. Artz, D. R. & Pi tts -Singer, T. L. Effects of fungicide and adjuvant sprays
on nesting behavior in two managed solitary bees, Osmia lignaria and Megachile rotundata. PLoS One 10, e0135688 (2015).
9. Atkins, E. L. & Kel lum, D. Comparative morphogenic and toxicity
s tudies on the effect of pesticides on honeybee brood. Journal of Apicultural Research 25, 242–255 (1986).
10. Mussen, E. C., Lopez, J. E. & Peng, C. Y. S. Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environmental Entomology 33, 1151–1154 (2004).
11. Heylen, K., Gobin, B., Arckens, L., Huybrechts, R. & Bi llen, J. The
effects of four crop protection products on the morphology and ul trastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera. Apidologie 42, 103–116 (2011).
12. Everich, R., Schiller, C., Whitehead, J., Beavers, M. & Barrett, K.
Effects of captan on Apis mellifera brood development under field conditions in California almond orchards. J Econ Entomol 102, 20–29 (2009).
13. Ladurner, E., Bosch, J., Kemp, W. P. & Maini, S. Assessing delayed and acute toxicity of five formulated fungicides to Osmia lignaria Say and
Apis mellifera. Apidologie 36, 449–460 (2005). 14. Huntzinger, C. I ., James, R. R., Bosch, J. & Kemp, W. P. Laboratory
bioassays to evaluate fungicides for chalkbrood control in larvae of
the a l falfa leafcutting bee (Hymenoptera: Megachilidae). Journal of economic entomology 101, 660–667 (2008).
15. Huntzinger, C. I ., James, R. R., Bosch, J. & Kemp, W. P. Fungicide tests on adult a lfalfa leafcutting bees (Hymenoptera: Megachilidae). Journal of economic entomology 101, 1088–1094 (2008).
16. Malone, L. A., Scott‐Dupree, C. D., Todd, J. H. & Ramankutty, P. No
sub‐lethal toxicity to bumblebees, Bombus terrestris, exposed to Bt‐corn pol len, captan and novaluron. New Zealand Journal of Crop and Horticultural Science 35, 435–439 (2007).
17. Thompson, H. & Wi lkins, S. Assessment of the synergy and repellency of pyrethroid/fungicide mixtures. B Insectol 56, 131–134 (2003).
18. Johnson, R. M., Dahlgren, L., Siegfried, B. D. & El lis, M. D. Acaricide,
fungicide and drug interactions in honey Bees (Apis mellifera). PLoS One 8, (2013).
©Heather Grab ©Katherine Urban-Mead ©Katherine Urban-Mead
24
19. Zhu, W., Schmehl, D. R., Mullin, C. A. & Frazier, J. L. Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLOS ONE 9, e77547 (2014).
20. vanEngelsdorp, D. et al. “Entombed Pollen”: A new condition in honey bee colonies associated with increased risk of colony mortality. Journal of Invertebrate Pathology 101, 147–149 (2009).
21. McArt, S. H., Urbanowicz, C., McCoshum, S., Irwin, R. E. & Adler, L. S.
Landscape predictors of pathogen prevalence and range contractions in US bumblebees. Proc R Soc B 284, (2017).
22. Singh, N. Toxicity and compatibility of some commonly used
insectiicides with selected fungicides and herbicides against honey bee Apis mellifera L. (Govind Ballabh Pant University of Agriculture
and Technology; Pantnagar, 2003). 23. Rodrigues, C. G., Krüger, A. P., Barbosa, W. F. & Guedes, R. N. C. Leaf
ferti lizers affect survival and behavior of the Neotropical s tingless bee
Friesella schrottkyi (Mel iponini: Apidae: Hymenoptera). J Econ Entomol 109, 1001–1008 (2016).
24. Vandame, R. & Belzunces, L. P. Joi nt actions of deltamethrin and azole fungicides on honey bee thermoregulation. Neuroscience
Letters 251, 57–60 (1998). 25. Lefebvre, B. & Bassand, D. Bee selectivity of MAVRIK®(tau-fluvalinate)
in tank mix with ERIA®(Difenoconazole, Ergosterol Biosynthesis Inhibitor-EBI). Short, medium and long term effects under semi-fields conditions. COLLOQUES-INRA 71–78 (2001).
26. Biddinger, D. J. et al. Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS ONE 8, e72587 (2013).
27. Albert, J. L. Field-level fungicide exposure and repellency to honey bees Apis mellifera during orchard bloom in Michigan. (Michigan
State University, 2018). 28. Pi l ling, E. D. Evidence for pesticide synergism in the honey bee (Apis
mellifera). Aspects of Applied Biology 31, 43–47 (1992). 29. Pi l ling, E. D. & Jepson, P. C. Synergism between EBI fungicides and a
pyrethroid insecticide in the honeybee (Apis mellifera). Pesticide science 39, 293–297 (1993).
30. European Food Safety Authority. Conclusion on the peer review of
the pesticide risk assessment of the active substance flutriafol. EFSA Journal 8, 1868 (2010).
31. Ra imets, R. et al. Synergistic interactions between a variety of insecticides and an ergosterol biosynthesis inhibitor fungicide in dietary exposures of bumble bees (Bombus terrestris L.). Pest
Managment Science 74, 541–546 (2018). 32. DEFRA, R. and D. Assessing the impact of mixtures of pyrethroids and
fungicides on honeybees. 1–20 (DEFRA, Central Science Laboratory, 2004).
33. Thompson, H. M., Fryday, S. L., Harkin, S. & Mi lner, S. Potential
impacts of synergism in honeybees (Apis mellifera,) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie 45, 545–553 (2014).
34. Sanchez-Bayo, F. & Goka, K. Pesticide residues and bees – a ri sk assessment. PLoS ONE 9, e94482 (2014).
35. Hawthorne, D. J. & Dively, G. P. Ki lling them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger
honey bees. PLOS ONE 6, e26796 (2011). 36. Iwasa, T., Motoyama, N., Ambrose, J. T. & Roe, R. M. Mechanism for
the di fferential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection 23, 371–378 (2004).
37. Johnson, R. M., Pol lock, H. S. & Berenbaum, M. R. Synergistic
interactions between in-hive miticides in <I>Apis mellifera</I>. Journal of Economic Entomology 102, 474–479 (2009).
38. Johnson, R. M., Wen, Z., Schuler, M. A. & Berenbaum, M. R. Mediation of pyrethroid insecticide toxicity to honey be es
(Hymenoptera: Apidae) by cytochrome P450 monooxygenases. Journal of economic entomology 99, 1046–1050 (2006).
39. Hagler, J. R., Waller, G. D. & Lewis, B. E. Mortality of honeybees (Hymenoptera: Apidae) exposed to permethrin and combinations of
permethrin with piperonyl butoxide. Journal of Apicultural Research 28, 208–211 (1989).
40. Zhu, Y. C., Yao, J., Adamczyk, J. & Luttrell, R. Synergistic toxicity and phys iological impact of imidacloprid a lone and binary mixtures with
seven representative pesticides on honey bee (Apis mellifera). PLoS One 12, e0176837 (2017).
41. Sgolastra, F. et al. Synergistic mortality between a neonicotinoid
insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Management Science 73, 1236–1243 (2017).
42. Robinson, A. et al. Comparing bee species responses to chemical mixtures: common response patterns? PLOS ONE 12, e0176289 (2017).
43. Steffan, S. A. et al. Empirical. Metagenomic, and Computational (2017).
44. Simone-Finstrom, M. Proceedings of the 2018 American Bee Research Conference. Bee World 95, 47–72 (2018).
45. Za luski, R., Justulin, L. A. & Ors i , R. de O. Field-relevant doses of the systemic insecticide fipronil and fungicide pyraclostrobin impair mandibular and hypopharyngeal glands in nurse honeybees (Apis mel lifera). Sci Rep 7, (2017).
46. Efrom, C. F. S., Redaelli, L. R., Meirelles, R. N. & Ourique, C. B. Side-
effects of pesticides used in the organic system of production on Apis mellifera Linnaeus, 1758. Brazilian Archives of Biology and Technology 55, 47–53 (2012).
47. Tomé, H. V. V. et al. Agrochemical synergism imposes higher ri sk to Neotropical bees than to honeybees. Royal Society Open Science 4,
160866 (2017). 48. Mull in, C. A. Effects of ‘inactive’ ingredients on bees. Curr Opin Insect
Sci 10, 194–200 (2015). 49. Carva lho, S. M., Carva lho, G. A., Carva lho, C. F., Bueno, C. F. &
Baptista, A. P. M. Toxici ty of acaricides/insecticides for ci trus crop to the africanized honeybee Apis mellifera L. São Paulo 76, 597–607 (2009).
50. Besard, L. et al. Compatibility of traditional and novel acaricides with bumblebees (Bombus terrestris): a first laboratory assessment of toxici ty and sublethal effects. Pest Manag Sci 66, 786–93 (2010).
51. Devi llers, J. et al. Comparative toxicity and hazards of pesticides to Apis and non-Apis bees. A chemometrical study. SAR QSAR Environ
Res 14, 389–403 (2003). 52. Naumann, K. & Isman, M. B. Toxicity of a neem (Azadirachta indica A.
Juss ) insecticide to larval honey bees. American Bee Journal (1996). 53. Xavier, V. M. et al. Acute toxicity and sublethal effects of botanical
insecticides to honey bees. J Insect Sci 15, (2015).
54. González-Gómez, R. et al. Effects of neem (Azadirachta indica) on honey bee workers and queens, while applied to control Varroa destructor. Journal of Apicultural Research 55, 413–421 (2016).
55. Barbosa, W. F., De Meyer, L., Guedes, R. N. C. & Smagghe, G. Lethal and sublethal effects of azadirachtin on the bumblebee Bombus terrestris (Hymenoptera: Apidae). Ecotoxicology 24, 130–142 (2015).
56. Mommaerts, V. & Smagghe, G. Side-effects of pesticides on the
pollinator Bombus: an overview. (In-Tech, 2011). 57. Marletto, F., Patetta, A. & Manino, A. Laboratory assessment of
pesticide toxicity to bumblebees. Bulletin of insectology 56, 155–158 (2003).
58. Fisher, A., Colman, C., Hoffmann, C., Fri tz, B. & Rangel, J. The effects
of the insect growth regulators methoxyfenozide and pyriproxyfen and the acaricide bifenazate on honey bee (Hymenoptera: Apidae)
forager survival. J Econ Entomol 111, 510–516 (2018).
25
59. El l is, M. D., Siegfried, B. D. & Spawn, B. The effect of Apistan® on honey bee (Apis mellifera L). Responses to methyl parathion, carbaryl and bifenthrin exposure. Apidologie 28, 123–127 (1997).
60. Pi l ling, E. D., Bromleychallenor, K. A. C., Walker, C. H. & Jepson, P. C.
Mechanism of synergism between the pyrethroid Insecticide λ -Cyhalothrin and the imidazole fungicide prochloraz, in the honeybee (Apis mellifera L.). Pesticide biochemistry and physiology 51, 1–11 (1995).
61. Col in, M.-E. & Belzunces, L. P. Evidence of synergy between prochloraz and deltamethrin in Apis mellifera L.: a convenient biological approach. Pesticide Science 36, 115–119 (1992).
62. Johansen, C. A., Mayer, D. F., Eves , J. D. & Kious, C. W. Pesticides and Bees. 12, 6 (1983).
63. Smagghe, G., Deknopper, J., Meeus, I . & Mommaerts, V. Dietary chlorantraniliprole suppresses reproduction in worker bumblebees. Pest management science 69, 787–791 (2013).
64. Kel ley, A. G., Ling-Hsiu, L. & Berenbaum, M. You are what you eat: food-drug interaction in honey bees (Apis mellifera). (2017).
65. Becker, R. Acute toxicity s tudy on the impact of chlorpyri fos and propiconazole in Apis mellifera. (University of Nebraska - Lincoln,
2016). 66. Thompson, H. M. Assessing the exposure and toxicity of pesticides to
bumblebees ( Bombus sp.). Apidologie 32, 305–321 (2001). 67. Gels, J. A., Held, D. W. & Potter, D. A. Hazards of insecticides to the
bumble bees <I>Bombus impatiens</I> (Hymenoptera: Apidae)
foraging on flowering white clover in turf. Journal of Economic Entomology 95, 722–728 (2002).
68. Uhl , P., Awanbor, O., Schulz, R. S. & Brühl, C. A. Osmia bicornis is
rarely an adequate regulatory surrogate species. Comparing its acute sensitivity towards multiple insecticides with regulatory Apis
mel lifera endpoints. bioRxiv 366237 (2018). doi :10.1101/366237 69. Bendahou, N., Bounias, M. & Fleche, C. Acute toxicity of
cypermethrin and fenitrothion on honeybees (Apis mellifera mellifera) according to age, formulations and (chronic paralysis vi rus )/insecticide interaction. J.Environ.Biol. 18, 55–65 (1997).
70. Cl inch, P. G. The residual contact toxicity to honey bees of insecticides sprayed on to white clover (Trifolium repens l .) in the
laboratory. New Zealand Journal of Agricultural Research 10, 289–300 (1967).
71. Ciarlo, T. J., Mul lin, C. A., Frazier, J. L. & Schmehl, D. R. Learning impairment in honey bees caused by agricultural spray adjuvants. PLOS ONE 7, e40848 (2012).
72. Gupta, P. R. & Chandel, R. S. Effects of diflubenzuron and penfluron on workers of Apis cerana indica F and Apis mellifera L. Apidologie 26,
3–10 (1995). 73. Tasei, J.-N. Effects of insect growth regulators on honey bees and
non-Apis bees. A review. Apidologie 32, 527–545 (2001).
74. Abramson, C. I ., Squire, J., Sheridan, A. & Mulder Jr, P. G. The effect of insecticides considered harmless to honey bees (Apis mellifera): proboscis conditioning s tudies by using the insect growth regulators tebufenozide and diflubenzuron. Environmental Entomology 33, 378–388 (2004).
75. Thompson, H. M., Wi lkins, S., Battersby, A. H., Waite, R. J. & Wi lkinson, D. The effects of four insect growth-regulating (IGR)
insecticides on honeybee (Apis mellifera L.) colony development, queen rearing and drone sperm production. Ecotoxicology 14, 757–
769 (2005). 76. Johnson, R. M. & Percel , E. G. Effect of a fungicide and spray adjuvant
on queen-rearing success in honey bees (Hymenoptera: Apidae). J
Econ Entomol 106, 1952–1957 (2013). 77. Emmett, B. J. & Archer, B. M. The toxicity of diflubenzuron to honey
bee (Apis mellifera L.) colonies in apple orchards. Plant Pathology 29, 177–183 (1980).
78. Steen, J. J. M. van der. The effect of the size of the bumble bee (Bombus terrestris L.) on the susceptibility to the pesticide dimethoate 40%. in Proceedings 7th international symposium of the ICPBR Bee Protection group: hazards of pesticides to bees at
Universite d’Avignon, France, 07-09 Septembre 1999 213–216 (2001). 79. Taséi, J.-N. & Dinet, P. Effets comparés de deux pyréthrinoides de
synthèse et de trois insecticides organophosphorés sur les mégachiles (Megachile rotundata F.= pacifica Pz.). Apidologie 12,
363–376 (1981). 80. Mayer, D. F., Lunden, J. D. & Kovacs , G. Susceptibility of four bee
species (Hymenoptera: Apoidea) to field weathered insecticide
res idues. Journal of the Entomological Society of British Columbia 94, 27–30 (1997).
81. Vidau, C. et al. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS one 6, e21550 (2011).
82. Stanley, J., Sah, K., Ja in, S. K., Bhatt, J. C. & Sushil, S. N. Eva luation of pesticide toxicity at their field recommended doses to honeybees, Apis cerana and A. mellifera through laboratory, semi-field and field s tudies. Chemosphere 119, 668–674 (2015).
83. Gradish, A. E., Scott-Dupree, C. D. & Cutler, G. C. Susceptibility of Megachile rotundata to insecticides used in wild blueberry production in Atlantic Canada. Journal of Pest Science 85, 133–140 (2012).
84. Gradish, A. E., Scott-Dupree, C. D., Frewin, A. J. & Cutler, G. C. Lethal
and sublethal effects of some insecticides recommended for wild blueberry on the pollinator Bombus impatiens. The Canadian Entomologist 144, 478–486 (2012).
85. Nation, J. L. & Robinson, F. A. Gibberellic acid: effects of feeding in an arti ficial diet for honeybees. Science 152, 1765–1766 (1966).
86. Marchetti, S., Barbattini, R. & D’AGARU, M. Comparative effectiveness of treatments used to control Varroa jacobsoni Oud. Apidologie 15, 363–378 (1984).
87. El l is, M. D. & Baxendale, F. P. Toxicity of seven monoterpenoids to tracheal mites (Acari: Tarsonemidae) and their honey bee (Hymenoptera: Apidae) hosts when applied as fumigants. Journal of Economic Entomology 90, 1087–1091 (1997).
88. Whittington, R., Winston, M. L., Melathopoulos, A. P. & Higo, H. A. Eva luation of the botanical oils neem, thymol, and canola sprayed to control Varroa jacobsoni Oud.(Acari: Varroidae) and Acarapis woodi (Acari : Tarsonemidae) in colonies of honey bees (Apis mellifera L., Hymenoptera: Apidae). American Bee Journal 140, 567–572 (2000).
89. Floris, I ., Satta, A., Cabras, P., Garau, V. L. & Angioni, A. Comparison between two thymol formulations in the control of Varroa
destructor: effectiveness, persistence, and residues. Journal of economic entomology 97, 187–191 (2004).
90. Imdorf, A., Bogdanov, S., Ochoa, R. I . & Calderone, N. W. Use of
essential oils for the control of Varroa jacobsoni Oud. in honey bee colonies. Apidologie 30, 209–228 (1999).
91. Leza, M., Watrous, K. M., Bratu, J. & Woodard, S. H. Effects of neonicotinoid insecticide exposure and monofloral diet on nest-founding bumblebee queens. Proc. R. Soc. B 285, 20180761 (2018).
92. Scott-Dupree, C. D., Conroy, L. & Harris, C. R. Impact of currently used or potentially useful insecticides for canola agroecosystems on
Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia l ignaria (Hymenoptera:
Megachilidae). Journal of Economic Entomology 102, 177–182 (2009). 93. Pashte, V. V. & Pati l, C. S. Impact of different insecticides on the
activi ty of bees on sunflower. Res Crops2017 18, 153–6 (2017).
94. Mayer, D. F., Kovacs , G. & Lunden, J. D. Field and laboratory tests on the effects of cyhalothrin on adults of Apis mellifera, Megachile
rotundata and Nomia melanderi. Journal of apicultural research 37, 33–37 (1998).
26
95. Torchio, P. F. Relative toxicity of insecticides to the honey bee, alkali bee, and a lfalfa leafcutting bee (Hymenoptera: Apidae, Halictidae, Megachilidae). Journal of the Kansas Entomological Society 446–453 (1973).
96. Drescher, W. & Geusen-Pfister, H. Comparative testing of the oral toxici ty of acephate, dimethoate and methomyl to honeybees, bumblebees and syrphidae. in VI International Symposium on Pollination 288 133–138 (1990).
97. Cutler, G. C. & Scott-Dupree, C. D. Novaluron: prospects and l imitations in insect pest management. Pest Technology 1.1 (2007).
98. Mommaerts, V., Sterk, G. & Smagghe, G. Hazards and uptake of chitin
synthesis inhibitors in bumblebees Bombus terrestris. Pest Management Science: formerly Pesticide Science 62, 752–758 (2006).
99. Hodgson, E. W., Pi tts -Singer, T. L. & Barbour, J. D. Effects of the insect growth regulator, novaluron on immature alfalfa leafcutting bees, Megachile rotundata. J Insect Sci 11, (2011).
100. Fine, J. D., Cox-Foster, D. L. & Mul l in, C. A. An inert pesticide adjuvant synergizes vi ral pathogenicity and mortality in honey bee larvae. Scientific Reports 7, 40499 (2017).
101. Thompson, H. M. & Hunt, L. V. Extrapolating from honeybees to
bumblebees in pesticide risk assessment. Ecotoxicology 8, 147–166 (1999).
102. Piccolomini, A. M., Whiten, S. R., Flenniken, M. L., O’Nei ll, K. M. & Peterson, R. K. D. Acute toxicity of permethrin, deltamethrin, and etofenprox to the a lfalfa leafcutting bee. J Econ Entomol 111, 1001–
1005 (2018). 103. Appel, A. G. Knockdown efficiency and materials’ compatibility of
wasp and hornet spray formulations to honey bees (Hymenoptera:
Apidae). Journal of economic entomology 83, 1925–1931 (1990). 104. Fourrier, J. et al. Larva l exposure to the juvenile hormone analog
pyriproxyfen disrupts acceptance of and social behavior performance in adult honeybees. PLOS ONE 10, e0132985 (2015).
105. Mommaerts, V., Sterk, G. & Smagghe, G. Bumblebees can be used in combination with juvenile hormone analogues and ecdysone agonists. Ecotoxicology 15, 513–521 (2006).
106. Mayes , M. A., Thompson, G. D., Husband, B. & Mi les, M. M. Spinosad toxici ty to pollinators and associated risk. in Reviews of
Environmental Contamination and Toxicology 179, 37–71 (Springer New York, 2003).
107. Morandin, L. A., Winston, M. L., Franklin, M. T. & Abbott, V. A. Lethal and sub-lethal effects of spinosad on bumble bees (Bombus
impatiens Cresson). Pest Manag Sci 61, 619–26 (2005). 108. Tomé, H. V. V., Barbosa, W. F., Martins, G. F. & Guedes, R. N. C.
Spinosad in the native stingless bee Melipona quadrifasciata: regrettable non-target toxicity of a bioinsecticide. Chemosphere 124,
103–109 (2015). 109. Kang, M. & Jung, C. Ecotoxicology of several acaricides used in apple
orchards to the honeybee, Apis mellifera : from the laboratory to the
field s tudy. Journal of Apiculture 25, 155–161 (2010). 110. Baptista, A. P. M., Carva lho, G. A., Carva lho, S. M., Carva lho, C. F. &
Bueno Filho, J. S. de S. Toxicity of pesticides used in citrus crop to Apis mellifera. Ciência Rural 39, 955–961 (2009).
111. Ramanaidu, K. Blueberry spanworm, Itame argillacearia (Packard)
and bumble bee, Bombus impatiens (Cresson) susceptibility to new biorational insecticides. (2011).
112. Maus , C. Ecotoxicological profile of the insecticide spirotetramat. Bayer CropScience Journal 23
113. El l is, C., Park, K. J., Whitehorn, P., David, A. & Goulson, D. The neonicotinoid insecticide thiacloprid impacts upon bumblebee colony development under field conditions. Environ. Sci. Technol. 51, 1727–1732 (2017).
114. Woodcock, B. A. et al. Country-specific effects of neonicotinoid
pesticides on honey bees and wild bees. Science 356, 1393–1395 (2017).
115. Els ton, C., Thompson, H. M. & Walters, K. F. A. Sub-lethal effects of
thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris)
micro-colonies. Apidologie 44, 563–574 (2013). 116. Sandrock, C. et al. Sublethal neonicotinoid insecticide exposure
reduces solitary bee reproductive success: Loss of pollinator fi tness. Agricultural and Forest Entomology 16, 119–128 (2014).
117. Coulon, M. et al. Metabolisation of thiamethoxam (a neonicotinoid pesticide) and interaction with the Chronic bee paralysis vi rus in honeybees. Pesticide Biochemistry and Physiology 144, 10–18 (2018).
An early spring solitary bee (Andrena sp.) collecting pollen
from the anthers of an apple flower
27
This document was prepared by the Dyce Lab of Honey Bee Studies, Cornell University ©2018
Sample Pollination Services Contract
This sample contract is provided as a service and is not a substitute for legal advice. This agreement dated ___________________ is made between the following parties: Beekeeper’s name: Grower’s name: __________________________________ ___________________________________
CONTACTINFORMATION Beekeeper Grower Mailing address: Phone number(s): Emergency phone number: Email address:
The parties agree to the following terms
CROPANDCOLONYOVERVIEW
This agreement involves the 20___ growing season Crop to be pollinated by honey bee colonies. This agreement is for crop varieties that are in flower.
Address and/or GPS coordinates of orchard/field where the hives will be placed
Date of colony placement* Date of colony removal* * If actual flowering dates differ from dates above, the grower will provide __ hours notice to the beekeeper regarding when colonies should be placed and removed No. of hives rented Price of a standard hive rental $ Total anticipated rental price $ Date(s) on which the rental fee is
payable to the beekeeper
Describe in detail or illustrate the colony placement in the orchard The grower will provide right of entry at all times to beekeepers visiting the property so that s/he can manage colonies
� Yes � No
Before services are provided, the beekeeper will locate a holding yard to place colonies in the event that they require movement to avoid a pesticide spray
� Yes � No
A water source will be provided to the honey bee colonies by the following party
� Beekeeper � Grower � No water will be provided
The grower and beekeeper agree to comply with all applicable federal, state and local laws, including pesticide label restrictions designed to protect bees.
The beekeeper agrees to provide colonies of the following standards:
COLONYSTATUSOFASTANDARDHIVEColony configuration (2 deeps, 1 deep, etc.) Minimum frames of bees in each hive Minimum frames of brood in each hive Pounds of food stores lbs Presence of a laying queen Colonies are free of American Foulbrood The beekeeper agrees to open and demonstrate the health and status of colonies randomly selected by the grower at least one (1) time following placement of the hives and thereafter as reasonably requested by the grower. The beekeeper will maintain colonies in good pollinating condition by providing feed, medication, and mite treatments as needed
28
This document was prepared by the Dyce Lab of Honey Bee Studies, Cornell University ©2018
The grower agrees to the following responsibilities:
GENERALRESPONSIBILITIESThe grower will provide a suitable place(s) for the hives that are accessible by truck or other vehicles The grower will hold the beekeeper harmless from any and all claims of injury or property damage arising from beekeeper’s performance of this contract, including but not limited to, claims arising from bee stings to animals or people, and claims for field or crop damage or loss resulting from the use of beekeepers vehicle(s).
MINIMIZINGRISKOFPESTICIDEEXPOSUREThe following pesticides or agricultural chemicals are mutually agreed to be used while the bees are on the crop: 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. The beekeeper will be notified of an application of a pesticide in this above list � Yes � No The beekeeper will be notified at the emergency contact (number/email address) provided above of an application of a pesticide that is not included in this above list
� Yes � No
The number of hours notice the grower agrees to give the beekeeper before a pesticide is applied to a crop (e.g., 48 hrs) hrs
If a pesticide not included in the above list will be applied during pollination, the grower shall assume the costs to move the colonies away from and back to the crop. State the cost of moving colonies
$
The grower will compensate the beekeeper for any colonies that died from acute pesticide poisoning events while present or within one month of pollinating this crop. Cause of death must be verified by the state apiculturist, state inspector, or Department of Environmental Conservation. State the cost of compensation per colony
$
The grower will dispose of all pesticide products in a manner that bees will not be able to contact it while searching for a source of water Additional agreements: ____________________________________________________________________________________________________________________________________________________________________________ ____________________________________________________________________________________________________________________________________________________________________________ ______________________________________________________________________________________ ______________________________________________________________________________________ ______________________________________________________________________________________ ______________________________________________________________________________________ ______________________________________________________________________________________ ______________________________________________________________________________________
ADDITIONALCONSIDERATIONSPrior to placing colonies for pollination, either party can terminate this contract should events occur beyond his/her control that prevent him or her from fulfilling the obligations as outlined (e.g., unexpected colony deaths, unexpected damage or disease of crops, etc.). If disputes arise that cannot be resolved through communication or small claims court, they will be settled by arbitration. Either party may request arbitration by providing written notice to the other at the contact information provided above by certified mail, return receipt requested. Within 10 days of receipt of such written request, each party will select one arbitrator and the two arbitrators will select a third. After reviewing the case, the decision of any two arbitrators will be binding. Cost of arbitration will be equally divided between the two parties. This contract shall be governed by New York law. Signature of beekeeper: ________________________________ Date: ______________ Signature of grower: ___________________________________ Date: ______________
29